Processing-dependent and clonal contamination patterns of Listeria monocytogenes in the cured ham food chain revealed by genetic analysis

Applied and Environmental Microbiology

Volumn 82, Issue 3, 2016, Pages 822-831

  Morganti, Marina ^a   Scaltriti, Erika ^a   Cozzolino, Paolo ^b   Bolzoni, Luca ^a   Casadei, Gabriele ^a   Pierantoni, Marco ^b   Foni, Emanuela ^a   Pongolini, Stefano ^a  

^a ISTITUTO ZOOPROFILATTICO SPERIMENTALE DELLA LOMBARDIA E DELL EMILIA ROMAGNA   (Italy)

^b Local Health Unit   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CHAINS; CLONING; CONTAMINATION; CURING; DISEASES; ELECTROPHORESIS; LISTERIA; MEATS;

CONTAMINATED SURFACES; ENVIRONMENTAL CONTAMINATION; GENETIC ANALYSIS; LISTERIA MONOCYTOGENES; PROCESSING FACILITIES; PULSED FIELD GEL ELECTROPHORESIS; ROUTINE MONITORING; SINGLE-NUCLEOTIDE POLYMORPHISMS;

MEATS; CONTAMINATION;

BACTERIUM; FOOD CHAIN; GENETIC ANALYSIS; GENETIC MARKER; HYGIENE; MEAT; THRESHOLD;

LISTERIA MONOCYTOGENES;

CLASSIFICATION; DEVICES; FOOD CHAIN; FOOD CONTROL; FOOD HANDLING; FOOD INDUSTRY; GENETICS; ISOLATION AND PURIFICATION; LISTERIA MONOCYTOGENES; LISTERIOSIS; MEDICAL DEVICE CONTAMINATION; MICROBIOLOGY; PROCEDURES; PULSED FIELD GEL ELECTROPHORESIS; RED MEAT; SINGLE NUCLEOTIDE POLYMORPHISM; STANDARDS; TRANSMISSION;

ELECTROPHORESIS, GEL, PULSED-FIELD; EQUIPMENT CONTAMINATION; FOOD CHAIN; FOOD HANDLING; FOOD MICROBIOLOGY; FOOD-PROCESSING INDUSTRY; LISTERIA MONOCYTOGENES; LISTERIOSIS; POLYMORPHISM, SINGLE NUCLEOTIDE; RED MEAT;

EID: 84957625946     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.03103-15     Document Type: Article

References (42)

1. EFSA, ECDC. 2015. The European Union summary report on trends and sources of zoonoses, zoonotic agents and foodborne outbreaks in 2013. EFSA J 13:3991.
2. Pinner RW, Schuchat A, Swaminathan B, Hayes PS, Deaver KA, Weaver RE, Plikaytis BD, Reeves M, Broome CV, Wenger JD. 1992. Role of foods in sporadic listeriosis. II. Microbiologic and epidemiologic investigation. The Listeria Study Group. JAMA 267:2046-2050.
3. Schuchat A, Deaver KA, Wenger JD, Plikaytis BD, Mascola L, Pinner RW, Reingold AL, Broome CV. 1992. Role of foods in sporadic listeriosis. I. Case-control study of dietary risk factors. The Listeria Study Group. JAMA 267:2041-2045.
4. Schuchat A, Swaminathan B, Broome CV. 1991. Epidemiology of human listeriosis. Clin Microbiol Rev 4:169-183.
5. Vazquez-Boland JA, Kuhn M, Berche P, Chakraborty T, Dominguez-Bernal G, Goebel W, Gonzalez-Zorn B, Wehland J, Kreft J. 2001. Listeria pathogenesis and molecular virulence determinants. Clin Microbiol Rev 14:584-640. http://dx.doi.org/10.1128/CMR.14.3.584-640.2001.
6. Pichler J, Much P, Kasper S, Fretz R, Auer B, Kathan J, Mann M, Huhulescu S, Ruppitsch W, Pietzka A, Silberbauer K, Neumann C, Gschiel E, de Martin A, Schuetz A, Gindl J, Neugschwandtner E, Allerberger F. 2009. An outbreak of febrile gastroenteritis associated with jellied pork contaminated with Listeria monocytogenes. Wien Klin Wochenschr 121:149-156. http://dx.doi.org/10.1007/s00508-009-1137-3.
7. Dalton CB, Austin CC, Sobel J, Hayes PS, Bibb WF, Graves LM, Swaminathan B, Proctor ME, Griffin PM. 1997. An outbreak of gastroenteritis and fever due to Listeria monocytogenes in milk. N Engl J Med 336:100-105. http://dx.doi.org/10.1056/NEJM199701093360204.
8. Aureli P, Fiorucci GC, Caroli D, Marchiaro G, Novara O, Leone L, Salmaso S. 2000. An outbreak of febrile gastroenteritis associated with corn contaminated by Listeria monocytogenes. N Engl J Med 342:1236-1241 http://dx.doi.org/10.1056/NEJM200004273421702.
9. Grif K, Hein I, Wagner M, Brandl E, Mpamugo O, McLauchlin J, Dierich MP, Allerberger F. 2001. Prevalence and characterization of Listeria monocytogenes in the feces of healthy Austrians. Wien Klin Wochenschr 113:737-742.
10. Farber JM, Peterkin PI. 1991. Listeria monocytogenes, a foodborne pathogen. Microbiol Rev 55:476-511.
11. McClure PJ, Kelly TM, Roberts TA. 1991. The effects of temperature, pH, sodium chloride and sodium nitrite on the growth of Listeria monocytogenes. Int J Food Microbiol 14:77-91. http://dx.doi.org/10.1016/0168-1605(91)90039-R.
12. Commission Regulation (EC). 2005. Commission regulation (EC) no. 2073/2005 of 15 November 2005 on microbiological criteria for foodstuffs. European Union, Brussels, Belgium. http://eur-lex.europa.eu/LexUriServ/LexUriServ.do?uri=OJ:L:2005:338:0001:0026:EN:PDF.
13. Prencipe VA, Rizzi V, Acciari V, Iannetti L, Giovannini A, Serraino A, Rossi A, Morelli D, Marino L, Migliorati G, Caporale V. 2012. Listeria monocytogenes prevalence, contamination levels and strains characterization throughout the Parma ham processing chain. Food Control 25:150-158 http://dx.doi.org/10.1016/j.foodcont.2011.10.018.
14. International Organization for Standardization (ISO). 2004. ISO 18593:2004 Microbiology of food and animal feeding stuffs. Horizontal methods for sampling techniques from surfaces using contact plates and swabs. International Organization for Standardization, Geneva, Switzerland. http://www.iso.org/iso/iso_catalogue/catalogue_tc/catalogue_detail.htm?csnumber=39849.
15. International Organization for Standardization (ISO). 2004. ISO 11290-1:1996/Amd.1:2004. Microbiology of food and animal feeding stuffs-horizontal method for the detection and enumeration of Listeria monocytogenes-part 1: detection method amendment 1: modification of the isolation media and the haemolysis test, and inclusion of precision data. International Organization for Standardization, Geneva, Switzerland. https://saz.isolutions.iso.org/obp/ui#iso:std:iso:11290:-1:ed-1:v1:amd:1:v1:en.
16. US Department of Agriculture, Food Safety and Inspection Service, Office of Public Health Science Laboratory Quality Assurance Division. 2013 Isolation and identification of Listeria monocytogenes from red meat, poultry and egg products, and environmental samples. USDA FSIS MLG 8.09, revision 9. US Department of Agriculture, Athens GA. http://www.fsis.usda.gov/wps/wcm/connect/1710bee8-76b9-4e6c-92fcfdc290dbfa92/MLG-8.pdf?MOD=AJPERES.
17. Centers for Disease Control and Prevention. 2013. Standard operating procedure for PulseNet PFGE of Listeria monocytogenes. Centers for Disease Control and Prevention, Atlanta, GA. http://www.cdc.gov/pulsenet/PDF/listeria-pfge-protocol-508c.pdf.
18. Andrews S. 2015. FastQC: a quality control tool for high throughput sequence data. http://www.bioinformatics.babraham.ac.uk/projects/fastqc/.
19. Chevreux B, Wetter T, Suhai S. 1999. Genome sequence assembly using trace signals and additional sequence information, p 45-46. In Computer science and biology: Proceedings of the German Conference on Bioinformatics (GCB), GCB '99. GCB, Hannover, Germany.
20. Ragon M, Wirth T, Hollandt F, Lavenir R, Lecuit M, Le Monnier A, Brisse S. 2008. A new perspective on Listeria monocytogenes evolution. PLoS Pathog 4:e1000146. http://dx.doi.org/10.1371/journal.ppat.1000146.
21. Gardner SN, Hall BG. 2013. When whole-genome alignments just won't work: kSNP v2 software for alignment-free SNP discovery and phylogenetics of hundreds of microbial genomes. PLoS One 8:e81760. http://dx.doi.org/10.1371/journal.pone.0081760.
22. Huelsenbeck JP, Ronquist F. 2001. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754-755. http://dx.doi.org/10.1093/bioinformatics/17.8.754.
23. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. 2011. MEGA5: Molecular Evolutionary Genetics Analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731-2739. http://dx.doi.org/10.1093/molbev/msr121.
24. Venables WN, Ripley BD. 2002. Modern applied statistics with S. Springer, New York, NY.
25. Brown L, Cat TT, DasGupta A. 2001. Interval estimation for a proportion. Stat Sci 16:101-133. http://dx.doi.org/10.1214/ss/1009213286.
26. Autio T, Hielm S, Miettinen M, Sjöberg AM, Aarnisalo K, Björkroth J, Mattila-Sandholm T, Korkeala H. 1999. Sources of Listeria monocytogenes contamination in a cold-smoked rainbow trout processing plant detected by pulsed-field gel electrophoresis typing. Appl Environ Microbiol 65:150-155.
27. Gudbjörnsdóttir B, Suihko M-L, Gustavsson P, Thorkelsson G, Salo S, Sjöberg A-M, Niclasen O, Bredholt S. 2004. The incidence of Listeria monocytogenes in meat, poultry and seafood plants in the Nordic countries. Food Microbiol 21:217-225. http://dx.doi.org/10.1016/S0740-0020(03)00012-1.
28. Zhao T, Podtburg TC, Zhao P, Schmidt BE, Baker DA, Cords B, Doyle MP. 2006. Control of Listeria spp. by competitive-exclusion bacteria in floor drains of a poultry processing plant. Appl Environ Microbiol 72: 3314-3320. http://dx.doi.org/10.1128/AEM.72.5.3314-3320.2006.
29. Brosch R, Chen J, Luchansky JB. 1994. Pulsed-field fingerprinting of listeriae: identification of genomic divisions for Listeria monocytogenes and their correlation with serovar. Appl Environ Microbiol 60:2584-2592.
30. Graves LM, Swaminathan B, Reeves MW, Hunter SB, Weaver RE, Plikaytis BD, Schuchat A. 1994. Comparison of ribotyping and multilocus enzyme electrophoresis for subtyping of Listeria monocytogenes isolates. J Clin Microbiol 32:2936-2943.
31. Piffaretti JC, Kressebuch H, Aeschbacher M, Bille J, Bannerman E, Musser JM, Selander RK, Rocourt J. 1989. Genetic characterization of clones of the bacterium Listeria monocytogenes causing epidemic disease. Proc Natl Acad Sci U S A 86:3818-3822. http://dx.doi.org/10.1073/pnas.86.10.3818.
32. Rasmussen OF, Skouboe P, Dons L, Rossen L, Olsen JE. 1995. Listeria monocytogenes exists in at least three evolutionary lines: evidence from flagellin, invasive associated protein and listeriolysin O genes. Microbiology 141(Pt 9):2053-2061. http://dx.doi.org/10.1099/13500872-141-9-2053.
33. Orsi RH, den Bakker HC, Wiedmann M. 2011. Listeria monocytogenes lineages: genomics, evolution, ecology, and phenotypic characteristics. Int J Med Microbiol 301:79-96. http://dx.doi.org/10.1016/j.ijmm.2010.05.002.
34. Doijad S, Weigel M, Barbuddhe S, Blom J, Goesmann A, Hain T, Chakraborty T. 2015. Phylogenomic grouping of Listeria monocytogenes. Can J Microbiol 9:1-10. http://dx.doi.org/10.1139/cjm-2015-0281.
35. Stasiewicz MJ, Oliver HF, Wiedmann M, den Bakker HC. 2015. Wholegenome sequencing allows for improved identification of persistent Listeria monocytogenes in food-associated environments. Appl Environ Microbiol 81:6024-6037. http://dx.doi.org/10.1128/AEM.01049-15.
36. Gilmour MW, Graham M, Van Domselaar G, Tyler S, Kent H, Trout-Yakel KM, Larios O, Allen V, Lee B, Nadon C. 2010. High-throughput genome sequencing of two Listeria monocytogenes clinical isolates during a large foodborne outbreak. BMC Genomics 11:120. http://dx.doi.org/10.1186/1471-2164-11-120.
37. Rychli K, Müller A, Zaiser A, Schoder D, Allerberger F, Wagner M, Schmitz-Esser S. 2014. Genome sequencing of Listeria monocytogenes "Quargel" listeriosis outbreak strains reveals two different strains with distinct in vitro virulence potential. PLoS One 9:e89964. http://dx.doi.org/10.1371/journal.pone.0089964.
38. Schmid D, Allerberger F, Huhulescu S, Pietzka A, Amar C, Kleta S, Prager R, Preussel K, Aichinger E, Mellmann A. 2014. Whole genome sequencing as a tool to investigate a cluster of seven cases of listeriosis in Austria and Germany, 2011-2013. Clin Microbiol Infect 20:431-436. http://dx.doi.org/10.1111/1469-0691.12638.
39. Wang Q, Holmes N, Martinez E, Howard P, Hill-Cawthorne G, Sintchenko V. 2015. It is not all about SNPs: comparison of mobile genetic elements and deletions in Listeria monocytogenes genomes links cases of hospital-acquired listeriosis to the environmental source. J Clin Microbiol 53:3492-3500. http://dx.doi.org/10.1128/JCM.00202-15.
40. Orsi RH, Borowsky ML, Lauer P, Young SK, Nusbaum C, Galagan JE, Birren BW, Ivy RA, Sun Q, Graves LM, Swaminathan B, Wiedmann M. 2008 Short-term genome evolution of Listeria monocytogenes in a noncontrolled environment. BMC Genomics 9:539. http://dx.doi.org/10.1186/1471-2164-9-539.
41. Vongkamjan K, Roof S, Stasiewicz MJ, Wiedmann M. 2013. Persistent Listeria monocytogenes subtypes isolated from a smoked fish processing facility included both phage susceptible and resistant isolates. Food Microbiol 35:38-48. http://dx.doi.org/10.1016/j.fm.2013.02.012.
42. Tenover FC, Arbeit RD, Goering RV, Mickelsen PA, Murray BE, Persing DH, Swaminathan B. 1995. Interpreting chromosomal DNA restriction patterns produced by pulsed-field gel electrophoresis: criteria for bacterial strain typing. J Clin Microbiol 33:2233-2239.